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A Cladistic Analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): Formerly the Phyla Pogonophora and Vestimentifera

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A Cladistic Analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): Formerly the Phyla Pogonophora and Vestimentifera Zoological Journal of the Linnean Society (2001), 132: 55–80. With 5 figures doi: 10.1006/zjls.2000.0263, available online at http://www.idealibrary.com on A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera GREG W. ROUSE School of Biological Sciences A08, University of Sydney, NSW 2006, Australia Received August 1999; accepted for publication June 2000 It has been proposed in recent years that the phyla Pogonophora and Vestimentifera are a derived clade of polychaete annelids. It has also been proposed that if this clade belongs among polychaetes, then the taxon name Pogonophora is misleading and should revert to a name first formulated for the group, Siboglinidae Caullery, 1914. This recommendation is adopted in this paper, and a cladistic study using terminals of ‘generic’ rank in the former Pogonophora (including Vestimentifera) is undertaken. The purpose of this is to assess which taxon names should now be used for clades within Siboglinidae, and to provide a revised taxonomy, based on phylogenetic principles. Another major aim is to assess the position of the vestimentiferan clade within Siboglinidae. The results show that Vestimentifera is the sister group to Sclerolinum, and this clade is then sister group to Frenulata, i.e. the remaining Siboglinidae. The results suggest that all taxa within Siboglinidae that are not genera or species are redundant, except for the following: Siboglinidae is defined as the first polychaete, and all its descendants, to have an gut occluded by expanded endoderm filled with chemoautotrophic bacteria, as seen in the holotype of Riftia pachyptila Jones, 1981. Monilifera can be defined based on apomorphy-based system such that it is the first siboglinid, and all its descendants, to have rings of chaetae (uncini) in the opisthosoma, as seen in the holotype of Sclerolinum magdalenae Southward, 1972. Vestimentifera can be defined as the first siboglinid and all its descendants to have a vestimentum as seen in the holotype of Riftia pachyptia. Frenulata is defined as the siboglinid, and all its descendants, to have a mid-trunk girdle, as seen in the holotype of Siboglinum weberi Caullery, 1914. The taxa of generic rank are not defined here since their monophyly was not investigated. 2001 The Linnean Society of London ADDITIONAL KEYWORDS: phylogenetic taxonomy – systematics – phylogeny – Monilifera – Frenulata. INTRODUCTION with reducing sediments, methane seeps, or with sunken terrestrial-plant debris. The varied and complex taxonomic history of Po- In his original description, Caullery (1914) noted gonophora and Vestimentifera represents one of the that Siboglinum weberi lacked an obvious digestive more fascinating tales in animal systematics. The fact tract, amongst other unusual features, and described that they tend to be found in deep-sea sediments it as having a dorsal nerve cord. He placed S. weberi resulted in the first member of this group, Siboglinum in a new family, Siboglinidae, but did not place it weberi Caullery, 1914, not being described until early within any other taxon, though he compared it with in the 20th century. There are now more than 100 deuterostomes such as hemichordates. Uschakov nominal species described, most from abyssal regions, (1933), apparently unaware of Caullery’s work, de- though exceptionally they are found in depths of less scribed a similar animal, Lamellisabella zachsi Us- than 100 m (Miura, Tsukahara & Hashimoto, 1997; chakov, 1933 from the north-eastern Pacific and placed Webb, 1964a). Some are large and spectacular mem- it in a new sabellid polychaete subfamily, Lamelli- bers of hydrothermal-vent communities (Jones, 1981a, sabellinae Uschakov, 1933. Johansson (1937, 1939) re- b), while others are smaller and found in association assessed the placement of L. zachsi, and decided it was not a polychaete. He erected a separate taxon name for it, Pogonophora, with the rank of class, but E-mail: [email protected] did not place it within any other taxon. Subsequent 55 0024–4066/01/050055+26 $35.00/0 2001 The Linnean Society of London 56 G. W. ROUSE workers (e.g. Beklemishev, 1944) then ranked Po- group, that of Siboglinidae Caullery, 1914. This name gonophora (with reference to Lamellisabella only) as change was also proposed by McHugh (1997) who, a phylum among deuterostomes. based on molecular sequence data on a variety of Ivanov (1951) compared Siboglinum and La- animals including a vestimentiferan, found that the mellisabella and was the first to recognize that both latter was nested among polychaetes. It has also been must belong to the same taxon and moved Siboglinum endorsed in two recent papers on the position of the weberi (and hence Siboglinidae) into Pogonophora. Iv- group (Halanych et al., 1998; Boore & Brown, 2000). anov (1952) described several new pogonophores and The suggestion by Rouse & Fauchald (1997) and later published a large monograph on the group (Iv- McHugh (1997) requires a reassessment of the utility anov, 1960, 1963). He regarded pogonophores as having of the current taxonomy of Pogonophora and Ves- deuterostome features such as radial cleavage, a dorsal timentifera, with both of these names treated, from nerve cord, and a tripartite coelom (formed by entero- this point on, as subsidiary to the name Siboglinidae. coely). Soon after, Webb (1964d) described the hitherto Here cladistic analyses are performed to assess which missing segmented, chaetal-bearing, posterior end taxon names should now be used for clades within (now called the opisthosoma). After this discovery some Siboglinidae. Another major aim is to assess the po- authors felt pogonophores were still deuterostomes sition of the vestimentiferan clade within Siboglinidae. (Ivanov, 1970, 1975a,b; Johansson, 1968), while others A new systematization, based on phylogenetic tax- suggested they were protostomes showing spiral cleav- onomy is then provided. age, a ventral nerve cord, chaetae and metameric segmentation (Liwanow & Porfirjewa, 1967; Nørre- BACKGROUND TO CURRENT SYSTEMATICS vang, 1970a,b; Southward, 1971b; George & South- Aspects of taxonomy within Siboglinidae (=Pogono- ward, 1973; van der Land & Nørrevang, 1975). phora and Vestimentifera) are briefly outlined here. The resolution of the placement of Pogonophora be- Further details are given in Table 1. Ivanov (1960, came more complicated with the description of La- 1963) divided the group referred to here as Frenulata mellibrachia barhami Webb, 1969a from slope depths (all Siboglinidae except for Sclerolinum and Ves- off California. Webb (1969a) placed L. barhami in a timentifera, see below) into Thecanephria and new pognophoran taxon, Vestimentifera. Later, closely Athecanephria. This was based on the development related taxa were found at hydrothermal vents, and of the anterior nephridial system. Unfortunately, it these massive worms were described by Jones (1981a, appears that the only taxa whose nephridia were in- b), who subsequently placed them in a separate vestigated by Ivanov were members of Siboglinum, phylum, Vestimentifera (Jones, 1985a). Jones (1985a) Oligobrachia (Ivanov, 1957) and Lamellisabella,and argued that, in spite of the many similarities between there is simply not enough information to assess the Vestimentifera and Pogonophora, Vestimentifera was utility of the nephridial system as a character. Never- more closely related to Annelida than to Pogonophora, theless, Ivanov (1960, 1963) used additional features thus justifying their separation. Southward (1988) con- such as spermatophore shape to justify his taxonomic sidered recognition of the phylum Vestimentifera as divisions. Within Athecanephria Ivanov (1960, 1963) untenable, and that vestimentiferans must belong in placed Oligobrachiidae Ivanov, 1957 with Birstenia the Pogonophora. This view was reinforced by Rouse Ivanov, 1952, Nereilinum Ivanov, 1961, Oligobrachia & Fauchald (1995) who listed eight synapomorphies Ivanov, 1957 (with Crassibrachia Southward, 1978a that grouped Pogonophora and Vestimentifera and and Unibrachium Southward, 1972 added later), and showed Jones’ (1985a) reasoning for erecting a phylum Siboglinidae with Siboglinum and Siboglinoides Iv- to be flawed. Molecular sequence data (Black et al., anov, 1961. Within Thecanephria he placed Poly- 1997; Kojima et al., 1997; Halanych, Lutz & Vrijenhoek, brachiidae Ivanov, 1952, with Cyclobrachia Ivanov, 1998) also suggest that Pogonophora and Ves- 1960, Diplobrachia Ivanov, 1960, Galathealinum Kir- timentifera form a monophyletic group. kegaard, 1956, Heptabrachia Ivanov, 1952, Poly- The idea postulated by Uschakov (1933) and Hart- brachia Ivanov, 1952, Sclerolinum Southward, 1961, man (1951, 1954) that Pogonophora are polychaetes and Zenkevitchiana Ivanov, 1957 [Choanophorus was revived by Bartolomaeus (1995), Nielsen (1995) Bubko, 1965 was added later, though this was then and Rouse & Fauchald (1995). Rouse & Fauchald questioned by (Webb, 1971)]; Lamellisabellidae with (1997) conducted a series of cladistic analyses of poly- Lamellisabella (and subsequently Siphonobrachia chaetes and showed that Pogonophora (including Ves- Nielsen, 1965), and Spirobrachiidae Ivanov, 1952 with timentifera) represents a member of a polychaete clade Spirobrachia Ivanov, 1952. This taxonomic system has called Sabellida. They argued that since the name remained largely unchanged, with the exception of the Pogonophora was misleading at this level, the name position of Sclerolinum (see below). of the group should revert to
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